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Ukrainian Journal of Ecology
Ukrainian Journal of Ecology, 2018, 8(4), 335-339
ORIGINAL ARTICLE
An association of Stenula bassarginensis (Gurjanova, 1948) (Crustacea: Amphipoda: Stenothoidae) and Tubularia cf. indivisa Linnaeus, 1758 (Cnidaria: Tubulariidae) in the coastal waters
of the Sea of Japan
I. Marin1,2, S. Sinelnikov3
A.N. Severtzov Institute of Ecology and Evolution of RAS, Moscow, 119071, Russia 2Biological Department, Altai State University, Barnaul, 656049, Russia, E-mail: [email protected] 3I.D. Papanin Institute for Biology of Inland Waters of RAS, Borok, Russia, E-mail: [email protected]
Received:22.10.2018. Accepted: 05.12.2018
Amphipod Stenula bassarginensis (Gurjanova, 1948) (Crustacea: Amphipoda: Stenothoidae) is described in association with oaten pipe hydroid Tubularia cf. indivisa Linnaeus, 1758 (Cnidaria: Tubulariidae) from Vostok Bay of the Sea of Japan and Busse lagoon in Aniva Bay of the Sea of Okhotsk (new record). Previously representative of the genus were known as associated of hermit crabs and anemones only.
Keywords: Hydrozoa; associations; hydroids; symbiosis; Amphipoda; Stenothoidae; Stenula Tubularia, Sea of Japan; Sea of Okhotsk
The amphipod family Stenothoidae Boeck, 1871 (Crustacea, Amphipoda) presently includes nearly 34 genera and about 200 known valid species of mostly symbiotic marine benthic amphipods recorded from subtidal communities to depths of more than 3000 meters (Barnard & Karaman, 1991; Bellan-Santini, 2005; Desbruyeres et al., 2001; Gurjanova, 1951; Horton et al. 2013; Krapp-Schickel & Koenemann, 2006; Krapp-Schickel, 1976, 2006, 2009, 2011, 2015; Tandberg & Vader, 2009; Krapp-Schickel & Brutto, 2015; Krapp-Schickel & Vader, 2015; Vader & Tandberg, 2013, 2015; WoRMS). Representatives of the family are known to be associated with different large marine invertebrates such as hydroids (Pirlot, 1932, Krapp-Schickel, 1993, Vader & Krapp-Schickel, 1996, Krapp-Schickel & Vader, 2015, Tandberg & Vader, 2015; Marin & Sinelnikov, 2017, 2018), sea anemones (Vader 1984, Vader & Krapp-Schickel, 1996, Krapp-Schickel & Vader, 1998), bivalves (Vader, 1972, Vader & Beehler, 1983; Tandberg et al., 2010), hermit crabs and other crustaceans (McGrath 1978, Thomas & Cairns, 1984, Marin & Sinelnikov, 2012, 2016, Marin et al., 2013). Nevertheless, the diversity, ecology and range of associations of these animals are not well studied. Most of stenothoid species are just morphologically described without any data on their ecology. Stenothoides bassarginensis Gurjanova, 1948 was described based on specimens collected in the Peter the Great Bay and Tatar Strait of the Sea of Japan (Gurjanova, 1948). No data on the ecology of the species were presented and since the description the species has not been reported in scientific literature or re-described. During the sampling in Vostok Bay and Aniva Bay of the Sea of Japan at the depth from 3-5 meters large stenothoids were found on hydrants of oaten pipe hydroid Tubularia cf. indivisa Linnaeus, 1758 (Cnidaria: Tubulariidae) (Fig. 1). Careful identification revealed that they belong to Stenula bassarginensis (Gurjanova, 1951) (Crustacea: Amphipoda: Stenothoidae) clearly identifying by the chela of gnathopods II.
Materials and methods
The collection of the material has been accomplished in coastal waters of the Vostok Bay of the Sea of Japan in July 2013 and the Busse Lagoon (southern Sakhalin Island) in the Aniva Bay of the Sea of Okhotsk in summer of 2014. Hydroids were photographed in situ and then collected underwater using SCUBA equipment. Underwater hydroid colonies were carefully separated from the substrate and placed in sealed plastic bags, eliminating the loss of symbionts. Flushing of symbionts from hydroids was carried out in the laboratory through a net with a diameter of a screen of 70 pm with a 5-10% solution of ethanol. Further, the collected animals and colonies were fixed in 70% solution of ethanol. The photos were done using the digital camera Canon PowerShot G11 and stereomicroscope Olympis with the digital camera.
Processing of material was carried out at A.N. Severtsov Institute of Ecology and Evolution of RAS, Moscow. The symbiotic assemblage from each colony was viewed under the binocular microscope; fixed animals were sorted into groups. The amphipod species identification was carried out according to Guryanova (1951). Only primary synonyms are given. The material is deposited in the author's collection at A.N. Severtsov Institute of Ecology and Evolution of RAS, Moscow (LEMMI).
Results
Family Stenothoidae Boeck, 1871 Genus StenulaJ.L. Barnard, 1962
Remarks. The type species - Stenula latipes (Chevreux & Fage, 1925) (== Stenothoides latipes Chevreux & Fage, 1925). The genus presently includes 16 valid species (after Krapp-Schickel & Vader, 2015) known from the Northern Atlantic (4 species), North Western Pacific (9 species), North Eastern Pacific (2 species) and Arctic (1 species).
Short diagnosis. Antenna 1 lacking nasiform process on article 1; accessory flagellum absent; palp of mandible 1 -articulate; palp of maxilla 1 1 -articulate; inner plate of maxilla 2 ordinary; inner plates of maxillipeds well separated. Gnathopod 1 small, almost simple, article 4 incipiently chelate; article 5 elongate, unlobed; article 6 almost linear. Gnathopod 2 slightly enlarged, palm weakly oblique, article 5 short, lobed. The genus Stenula possesses only pereopod 3 with slender article 2 and pereopods 4-5 with broad and inflated article 2. The main difference of the relative genus Stenothoides is in morphology of article 2 of pereopods 3-5: the latter species possess pereopods 3-4 with slender article 2 and only pereopod 5 with expanded article 2 (after Barnard, 1962).
Stenula bassarginensis (Gurjanova, 1948) (Figs. 1f g, 2)
Stenothoides bassarginensis Gurjanova, 1948: 314, fig. 19 [type locality - Sea of Japan]. Stenula bassarginensis. - Barnard, 1962: 137.
Material examined. 7 ovigerous females, 5 males (LEMMI) - Sea of Japan, Vostok Bay, in front of scientific station "Vostok", 42°53'36.0"N 132°43'54.0", 3-5 m, on Tubularia cf. indivisa, SCUBA, coll. I. Marin, July 2013; 3 ovigerous females, 2 males (LEMMI) - Sea of Okhotsk, Aniva Bay, Busse Lagoon, 46°32'42.2"N 143°21'10.4"E, 1-3 m, on Tubularia cf. indivisa, SCUBA, coll. I. Marin, 2014.
Remarks. The specimens of S. bassarginensis (Fig. 2) clearly belong to described by Gurjanova (1948, 1951) and can be identified by characteristic margin of chela of gnathopod 2 (Fig. 2c f). The species belong to the genus Stenula after Barnard's (1962) genera recognition possessing pereopod 3 with slender article 2 and pereopods 4 and 5 with broad and inflated article 2 (Fig. 2a). Krapp-Schickel & Vader (2015) provided a key to all known species of the genus Stenula.
Host and ecology. The species was found in association with large oaten pipe hydroid Tubularia cf. indivisa Linnaeus, 1758 (Cnidaria: Tubulariidae) (Fig. 1a-e) both in Vostok Bay and Busse lagoon of Aniva Bay. Large specimens (possibly females) usually occupy the hydrants of hydroids solitary with a lot of small juveniles (see Fig. 1 d, e). The ecology of the species is probably similar to Metopa alderi(Bate, 1857) (Crustacea: Amphipoda: Stenothoidae) associated with Ectopleura larynx(Ellis, Solander, 1786) (Cnidaria: Tubulariidae) in the White Sea (see Marin & Sinelnikov, 2017). Representatives of the genus Stenula are known in associations with hermit crabs (S. latipes after McGrath, 1978) and sea anemones (S. solsbergi and S. pugilla after Krapp-Schickel & Vader, 2015). Another amphipod species found in the same samples is Ischyrocerus cf. enigmaticus Gurjanova, 1934 (Amphipoda: Ishyroceridae).
Distribution. The species is known exclusively in the Sea of Japan from Tatar Strait to the Peter the Great Bay (Gurjanova, 1948) and Busse lagoon of Sakhalin Island in Aniva Bay of the Sea of Okhotsk (new record).
Acknowledgements
Authors are grateful to the staff of the National Scientific Center of Marine Biology FEB RAS, Vladivostok, the staff and the director of the Marine Biological Station "Vostok". Authors are also sincerely grateful to PhD A.S. Mayorova for her assistance in collection of the material at Sakhalin Island.
References
Barnard, J.L. (1962). Benthic marine Amphipoda of southern California. 3. Families Amphilochidae, Leucothoidae, Stenothoidae, Argissidae, Hyalidae. Pacific Naturalist, 3(3), 116-163.
Barnard, J.L. & Karaman, G.S. (1991). The families and genera of marine gammaridean Amphipoda (except marine gammaroids). Records of the Australian Museum, Supplement, 13, 1-866.
Bellan-Santini, D. (2005). Stenothoidae (Crustacea: Amphipoda) of hydrothermal vents and surroundings on the Mid-Atlantic Ridge, Azores Triple Junction zone. Journal of Natural History, 39(39), 3435-3452.
Desbruyeres, D., Biscoito, M., Caprais, J.C., Colaco, A., Comtet, T., Crassous, P., Fouquet, Y., Khripounoff, A., Le Bris, N., Olu, K., Riso, R., Sarradin, P.M., Segonzac, M. & Vangriesheim, A. (2001). Variations in deep-sea hydrothermal vent communities on the Mid-Atlantic Ridge near the Azores plateau. Deep-Sea Research I, 48, 1325-1346.
Gurjanova, E.F. (1951). Amphipods of the seas of the USSR and surrounding waters (Amphipoda-Gammaridea). Opredeliteli po faune SSSR, 41, 1-1029 (in Russian).
Horton, T., De Broyer, C., Costello, M., Bellan-Santini, D. (2013). Stenothoidae. In: Horton, T., Lowry, J., De Broyer, C., Bellan-Santini, D., Coleman, C. O., Daneliya, M., Dauvin, J-C., Fiser, C., Gasca, R., Grabowski, M., Guerra-García, J. M., Hendrycks, E., Holsinger, J., Hughes, L., Jaume, D., Jazdzewski, K., Just, J., Kamaltynov, R. M., Kim, Y.-H., King, R., Krapp-Schickel, T., LeCroy, S., Lorz, A.-N., Senna, A. R., Serejo, C., Sket, B., Tandberg, A.H., Thomas, J., Thurston, M., Vader, W., Vainola, R., Vonk, R., White, K.
& Zeidler, W. (2017). World Amphipoda Database. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=101409 on 2017-10-07 Krapp-Schickel, G. (1976). Die Gattung Stenothoe im Mittelmeer. BijdrDierkunde, 46, 1-34.
Krapp-Schickel, T. (1993). Family Stenothoidae. In: Ruffo, S. (ed.): The Amphipoda of the Mediterranean. Part 3. Memoires de l'Institut oceanographique. Monaco, 13, 692-709.
Krapp-Schickel, T. (2006). New Australian Stenothoids (Crustacea, Amphipoda) with key to all Stenothoe species. Bollettino del Museo Civico di Storia Naturale di Verona Botanica Zoologia, 3, 39-56.
Krapp-Schickel, T. (2009). New and poorly described stenothoids (Crustacea, Amphipoda). from the Pacific Ocean. Memoirs of Museum Victoria, 66, 95-116.
Krapp-Schickel, T. (2011). New Antarctic stenothoids sensu lato (Amphipoda, Crustacea). European Journal of Taxonomy, 1, 117.
Krapp-Schickel, T. (2015). Minute but constant morphological differences within members of Stenothoidae: the Stenothoe gallensis group with four new members, keys to Stenothoe worldwide, a new species of Parametopa and Sudanea n. gen. (Crustacea: Amphipoda). Journal of Natural History, 40(37-38), 2309-2377.
Krapp-Schickel, T. & Lo Brutto, S. (2015). Two new Mediterranean Stenothoe (Crustacea, Amphipoda) from the coast of Israel. Marine Biodiversity Records, 8, e84, 1 -5.
Krapp-Schickel, T. & Koenemann, S. (2006). Cladistic analysis of the family Stenothoidae (Amphipoda, Crustacea). Contributions to Zoology, 75(3/4), 169-188.
Krapp-Schickel, T., & Vader, W. (1998). A new Parametopella species (Crustacea: Amphipoda: Stenothoidae) from Antholoba achates(Anthozoa: Actiniaria) from Coquimbo, Chile (with remarks on Parametopa alaskensis(Holmes)). Journal of the Marine Biological Association of the United Kingdom, 89, 1281 -1287.
Krapp-Schickel, T. & Vader, W. (2015). Stenothoids living with or on other animals (Crustacea, Amphipoda). Zoosystematics & Evolution, 91 (2), 215-246.
Marin, I. & Sinelnikov, S. (2012). Metopelloidespagurisp. nov., a new species of symbiotic stenothoid amphipod (Crustacea:
Amphipoda: Stenothoidae) associated with sublittoral hermit crabs in the Sea of Japan. Zootaxa, 3244, 59-67.
Marin, I.N. & Sinelnikov, S.Yu. (2016). Diversity and ecological features of symbiotic communities associated with large hermit
crabs along the southern part of the Russian coast of the Sea of Japan. Arthropoda Selecta, 25(2), 171 -182.
Marin, I.N. & Sinelnikov, S.Y. (2017). Amphipod assemblage found on sublittoral hydroids in the White Sea with the special
remarks to symbiotic association of stenothoid Metopa alderi with hydroid Tubularia larynx. Ukrainian Journal of Ecology, 7(4),
473-479.
Marin, I. & Sinelnikov, S. (2018). Two new species of amphipod genus Stenothoe Dana, 1852 (Stenothoidae) associated with fouling assemblages from Nhatrang Bay, Vietnam. Zootaxa, 4410(1), 57-76.
Marin, I., Sinelnikov, S. & Sokolova, A. (2013). Ecological remarks and re-description of the hermit crab-associated pleustid amphipod Pleusymtes japonica (Gurjanova, 1938) (Crustacea: Amphipoda: Pleustidae: Pleusymtinae) from the Sea of Japan. Zootaxa, 3640(4), 581 -588.
McGrath, D. (1978). Stenula latipes (Chevreux and Fage) (Crustacea: Amphipoda), associated with the hermit crab Pagurus bernhardus (L.), new to the Irish fauna. Irish Naturalists 'Journal, 19, 196-197.
Pirlot, J.M. (1932). Sur quelques amphipodes associes aux colonies de tubulaires dans la region de Bergen. Bulletin duSociete royal des Sciences de Likge, 2, 21 -27.
Tandberg, A.H.S. & Vader, W. (2015). Stenothoidae associated with hydroids - does association with other taxa trigger extended parental care? In: Abstracts of 16Th International colloquium on Amphipoda, Aveiro, 7-11 September 2015. UA Edttora, Portugal, 14.
Tandberg, A.H.S., Schander, C. & Pleijel, F. (2010). First record of the association between the amphipod Metopa alderii and the bivalve Musculus. Marine Biodiversity Records (2010), 3, e5.
Thomas, J.D. & Cairns, K.D. (1984). Discovery of a majid host for the commensal amphipod Stenothoe symbiotica Shoemaker, 1956. Bulletin of Marine Science, 34(3), 484-485.
Vader, W. (1972). Associations between amphipods and mollusks. A review of published records. Sarsia, 48, 13-18.
Vader, W. (1984). Associations between amphipods (Crustacea: Amphipoda) and sea anemones (Anthozoa: Actiniaria).
Australian Museum Memoir, 18(13), 141 -153.
Vader, W. & Krapp-Schickel, G. (1996). Redescription and biology of Stenothoe brevicornis Sars (Amphipoda: Crustacea), an obligate associate of the sea anemone Actinostola callosa(Verrill). JournalofNaturalHistory, 30, 51-66. Vader, W. & Tandberg, A.H.S. (2013). A survey of amphipods associated with molluscs. Crustaceana, 86(7-8), 1038-1049. Vader, W. & Tandberg, A.H.S. (2015). Amphipods as associates of other Crustacea: a survey. Journal of Crustacean Biology, 35(4), 522-532.
Vader, W. & Beehler, C.S. (1983). Metopa glacialis (Amphipoda, Stenothoidae) in the Barents and Beaufort Seas, and its association with the lamellibranchs Musculusnigerand M. discors. l. Astarte, 12 (1979), 57-61.
Citation:
Marin, I., Sinelnikov, S. (2018). An association of Stenula bassarginensis(Gur\anova, 1948) (Crustacea: Amphipoda: Stenothoidae) and Tubularia cf. indivisa Linnaeus, 1758 (Cnidaria: Tubulariidae) in the coastal waters of the Sea of Japan. Ukrainian Journal of Ecology, 8(4), BBS-SB^_
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Figure 1. Stenula bassarginensis on its host Tubularia cf. indivisa Linnaeus, 1758: a-c- general view of hydroid colonies in situ, d, e- hydrants with amphipods in situ (probably female and group of juveniles); f g- photo of S. bassarginensis on hydrants made in laboratory
Figure 2. Stenula bassarginensis(Gurjanova, 1948): a, b - mature male, general view; c f- gnathopod 2; d e- mature females, general view; g- juvenile.
